Journal of Applied Microbiology 2003, 94, 87S–93S
Overland flow transport of pathogens from
agricultural land receiving faecal wastes
S.F. Tyrrel1 and J.N. Quinton2
1
Institute of Water and Environment, Cranfield University, Silsoe Bedford, and 2Department of Environmental
Science, Institute of Environmental and Natural Sciences, Lancaster University, Lancaster, UK
1. Summary, 87S
2. Introduction, 87S
3. Faecal pathogens in soils, 88S
3.1 Sources, 88S
3.2 Survival in soil, 89S
4. Overland flow transport of microorganisms, 89S
4.1 Empirical transport models, 89S
4.2 Pathogen transport processes, 90S
1. SUMMARY
Considerable investment has been made in recent years in
improvements to the microbiological quality of urban
wastewater discharges to surface waters, particularly in
coastal towns, with the aim of reducing the exposure of
bathers and surfers to gastrointestinal pathogens. As this
source of pollution has come under greater control, attention
has started to focus on diffuse catchment sources of faecal
contamination which have been shown to be dominant
during high river flows associated with storm events. This
association with storm events suggests that rapidly responding hydrological pathways such as overland flow are likely to
be important. The aim of this paper is to establish the
current state of knowledge of pathogen transport processes
in overland flow. In addition, the paper will attempt to
convey the way that soil erosion science may aid our
understanding of this environmental problem. The scale and
nature of faecal waste applications to land in the UK is
briefly reviewed, with data presented on both livestock
slurry and manure, and human sewage sludge. Particular
emphasis is placed on factors influencing the likelihood of
pathogens making their way from infected livestock and
humans to the soil surface, and therefore the chances of
them being available for transport by overland flow. The
literature relating to pathogen transport in overland flow is
reviewed. Existing pathogen transport models treat pathogens as particles and link pathogen transport models to
Correspondence to: S.F. Tyrrel, Institute of Water and Environment,
Cranfield University, Silsoe, Bedford MK45 4DT, UK
(e-mail:[email protected]).
ª 2003 The Society for Applied Microbiology
4.2.1 Initial and boundary conditions, 90S
4.2.2 Initiation of overland flow, 90S
4.2.3 Entrapment of microorganisms in overland
flow, 90S
4.2.4 Transport and deposition, 91S
5. Conclusions, 91S
6. Acknowledgements, 92S
7. References, 92S
pathogen die-off kinetics. Such models do not attempt to
describe the interactions that may occur between pathogens
and soil and waste particles. Although conceptual models
describing the possible states in which pathogen transport
may occur have been proposed, an understanding of the
factors controlling the partitioning of the microorganisms
between the different states is only just beginning to emerge.
The apparent poor performance of overland flow mitigation
measures such as grass buffer strips in controlling the
movement of faecal indicators highlights the need for a
better understanding the dynamics of microbial transport so
that better management approaches may be developed.
Examples of on-going research into overland flow transport
processes are briefly described and gaps in knowledge
identified.
2. INTRODUCTION
The introduction of the EC Bathing Waters Directive (76/
160/EEC) [Council of the European Communities (CEC)
1976] focused attention on the causes on faecal contamination of natural waters. Discharges of untreated or partially
treated urban wastewater from coastal towns into the sea
were initially thought to be the principal cause of failure to
meet the microbiological standards set out in the directive to
protect the health of recreational water users at designated
bathing sites. However, a series of studies (Wyer et al. 1996,
1998; Kay et al. 1999; Baudart et al. 2000) have demonstrated that whereas urban wastewater dominates faecal loads to
bathing waters during low flow conditions, catchment
sources of faecal pollution become the dominant input
following rainfall events. These catchment sources of faecal
88S S . F . T Y R R E L A N D J . N . Q U I N T O N
pollution may include sewage sludge and livestock wastes
applied to land; animal faeces deposited on land by grazing
animals; discharges from septic tank systems; and defaecation by indigenous fauna (Wyer et al. 1994, 1996; Geldreich
1996; Jones and Obiri-Danso 1999; Obiri-Danso and Jones
1999). The observed link between rainfall, channel flow
conditions and the dominance of diffuse sources of faecal
pollution in catchment budgets suggests a key role for
hydrological pathways that respond rapidly to storm events.
One such pathway is overland flow. Overland flow occurs
when rainfall is unable to infiltrate the soil surface and runs
over the ground, normally in rivulets. Overland flow is of
considerable interest to researchers studying diffuse pollution because it is the predominant means by which soil
particles are transported from land to surface waters. The
transport of soil particles can have deleterious effects on
water quality such as bed siltation and increased turbidity.
Furthermore, much has been learned in recent years of the
potential for pollutants with a propensity for adsorption to
soil particles (such as pesticides and phosphate) to be
transported to watercourses in overland flow. It has also
been recognized that faecal indicator bacteria and associated
pathogens may be transported in overland flow (Van Donsel
et al. 1967; McCaskey et al. 1971; Doran and Linn 1979;
Khaleel et al. 1980; Crane et al. 1983; Patni et al. 1985;
Mawdsley et al. 1995; Tate et al. 2000) and that this may be
a significant cause of surface water contamination. Given the
potential impacts of surface water contamination by faecal
pathogens, understanding the processes by which microorganisms are transported from soils to waters is important if
we wish to build process-based predictive tools or to design
strategies to prevent the bacterial contamination of surface
waters. The aim of this paper is to establish the current state
of knowledge of pathogen transport processes in overland
flow. The review will describe in general terms, the
approaches commonly used in the study of soil erosion
processes are being applied to this environmental microbiology problem.
of tillage land receives slurry in any 1 year in England and
Wales (Nicholson et al. 2000). Livestock faecal wastes may
contain pathogenic microorganisms such as Listeria, Campylobacter, Salmonella, Escherichia coli 0157, Cryptosporidium
and Giardia (Hinton and Bale 1991; Mawdsley et al. 1995;
Pell 1997; Nicholson et al. 2000). Nicholson et al. (2000) in
their review of risks of pathogen transfer into the food chain
from manure applications to land state that there is a lack of
data on typical levels of pathogens in animal manures.
Examples of reported incidence of key zoonotic pathogens in
the faeces of cattle are presented in Table 1.
Prevalence of infection is only one of the factors
influencing likelihood of pathogens being available at the
soil surface for transport by overland flow. The actual
numbers of pathogens shed is important and this has been
found to be affected by a number of factors such as animal
age, diet, stress and season (Nicholson et al. 2000). The
probability of pathogens being available for transport at
the soil surface is also likely to be influenced significantly by
the duration and conditions of storage prior to land
spreading. Although the Code of Good Agricultural Practice
for the Protection of Water (MAFF 1998) recommends that
a storage tank should hold at least 4-month slurry, in
practice storage periods may be significantly less than that
recommended as stores built before 1991 are usually exempt
from the regulations. The environmental conditions that
have been found to most significantly affect pathogen
survival in storage have been identified in the review by
Nicholson et al. (2000). This review concluded that
temperature is the single most important factor which
determines pathogen survival times in livestock manures.
Other factors found to affect pathogen survival include
ammonia, high pH, desiccation and competition. The
method of waste storage will determine these conditions.
For example, faecal wastes that have been subject to the
manuring process are less likely to have high pathogen loads
because of the combination of relatively high temperatures
and long storage periods associated with this low-rate
composting process. Recent trials in the UK have demonstrated that whilst pathogens could survive for up to
3. FAECAL PATHOGENS IN SOILS
3.1 Sources
Large amounts of animal faecal wastes are applied to
agricultural land in the UK. Nicholson et al. (2000) estimate
that approximately 68 million tonnes (wet weight) were
produced by housed livestock in 1997 in England and Wales,
most of which is recycled back to agricultural land because
of its fertilizer value. Approximately three-quarters of these
wastes are produced by cattle and the remainder by sheep,
pigs and poultry. Some 41% of faecal wastes will be in the
form of either slurry (including dirty water) and 59% as
farm yard manure (FYM). About 15% of grassland and 3%
Table 1 Examples of reported incidence of key zoonotic pathogens in
the faeces of cattle
Pathogen
Incidence in faecal
samples (%)
Campylobacter spp.
89
Listeria monocytogenes 16
E. coli O157
1–5
1–15
Salmonella spp.
23
Cryptosporidium spp. 48
Reference
Stanley et al. (1998)
Pell (1997)
Zhao et al. (1995)
Jones (1999)
Troutt et al. (2001)
Sturdee et al. (1998)
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PATHOGEN TRANSPORT IN OVERLAND FLOW
3 months in batched stored dairy slurry, they could not be
detected after 1 week in an unturned manure heap (Nicholson et al. 2002).
The need to treat urban wastewater to high standards
prior to discharge into receiving waters results in the
production of a residue known as sewage sludge, and this
requires disposal. Forecasts suggest that by 2005, the annual
production of sludge (dry solids) in the UK will be
approximately 1Æ5 million tonnes in the UK and 8Æ3 million
tonnes in the Europe as a whole. It is forecast that by 2005,
71% of this sludge will be recycled to agricultural land in
the UK (CEC 1999). The type and number of human
pathogens present in untreated sewage sludge will vary
according the prevalence of gastrointestinal disease in the
community that produces it (Smith 1996). Sewage sludge is
probably a less-important source of pathogen contamination
of soil than livestock slurry and manure, however, because of
the increasingly stringent operational restrictions on its use
in agriculture. For example, in the UK the Sludge (Use in
Agriculture) Regulations [Statutory Instrument (SI) UK
1989] which implement the Europe Sludge Directive 86/
278/EEC (CEC 1986) require that only sludges that have
been subjected to a recognized effective treatment process
such as storage for 3 months may be applied to agricultural
land. More recently, the Safe Sludge Matrix (http://
www.adas.co.uk/matrix/) – an agreement between the
water industry, food retailers and Government – will further
reduce the chances of sludge pathogens being available for
transport by overland flow. Key components of the Matrix
include a phasing out of untreated sewage sludge use on
agricultural land; restrictions on the use of conventionally
treated sludges on risky crop groups such as salads, fruit and
vegetables; and the requirement for enhanced treatment for
the aforementioned risky crop groups. Enhanced treated
sludge should be free from salmonellas (in five replicates of
2 g dried solids) and virtually free of other pathogens (as
indicated by a 6 log reduction in the number of E. coli).
It should be noted that human or livestock faecal wastes
are not the only potential source of transportable pathogens
at the soil surface. Doran and Linn (1979) reported faecal
coliform concentrations in runoff from ungrazed grassland
in the range 150–50 000 CFU 100 ml)1. Patni et al. (1985)
report similar findings and concluded that the faeces of wild
animals were probably the source of this contamination.
3.2 Survival in soil
The other major factor influencing the availability of wastederived pathogens for overland flow transport is their
survival in the soil environment. The survival in soil of
pathogens originating from animal manures and sewage
sludge has been reviewed by Van Donsel et al. (1967),
Sorber and Moore (1987), Smith (1996) and Nicholson et al.
89S
(2000). Although a number of environmental factors have
been shown to influence the survival of microorganisms in
soil (e.g. temperature, moisture content, sunlight, pH and
the availability of organic matter) these reviewers appear to
agree that temperature is the most significant. In general,
survival time increases with decreasing temperature.
Nicholson et al. (2000) conclude that the majority of
pathogens in manures applied to land will decline below
detectable limits after 3 months. Therefore more pathogens
are likely to be transported to a watercourse if an overland
flow event occurs soon after faecal waste is applied to land.
The way that faecal wastes are applied to the land may
also have a bearing on the survival and hence the chances of
pathogen transport to watercourses. Intuitively, we would
expect that faecal wastes spread onto the soil or crop surface
are more likely to be subject to detachment and transport
than wastes that have been injected below the soil surface or
incorporated in some way. Walker et al. (1990) in their
modelling work assume that only 50% of microorganisms
are available if manures are incorporated to a depth of
10 cm. On the other hand, the environment at the soil
surface may be more hostile because of the effects of
insolation (e.g. u.v. irradiation, heating and desiccation) than
the environment at depth. There is relatively little evidence
in the literature of studies that have addressed the question
of whether or not incorporation or injection will reduce
pathogen losses. In a comparative study of runoff of faecal
microorganisms and nutrients from grass plots that had
received either injected or surface-applied slurry HeinonenTanski and Uusi-Kämppä (2001) concluded that there was
no clear difference between application methods. Daniel
et al. (1995) found no significant difference in runoff quality
(no microbial indicators measured) between surface-applied
and incorporated manure. Small scale rainfall simulation
experiments conducted by the authors however suggest that
there is approximately a 10-fold increase in faecal coliform
transport if waste is surface-applied rather than incorporated
(unpublished data).
4. OVERLAND FLOW TRANSPORT
OF MICROORGANISMS
4.1 Empirical transport models
Most authors assume that microorganisms behave like soil
particles, making predictions of pathogen transport using
existing soil erosion models linked to models describing the
die-off of microorganisms contained in animal wastes and
manures before and after application to the soil. Once the
population in the soil is predicted, it is assumed that
the concentration can be multiplied by the soil loss to yield
the number of microorganisms transported. This approach
was used by Walker et al. (1990) who used the Modified
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90S S . F . T Y R R E L A N D J . N . Q U I N T O N
Universal Soil Loss Equation, an empirically based soil
erosion model, to predict faecal coliform transport from soils
amended with manures in the Owl Run catchment in
Virginia, USA. To calculate the sediment yield for a single
storm the model uses a number of empirically derived
factors based on soils and topography combined with
predicted peak and total runoff. The number of bacteria
transported is calculated by assuming that a constant
number of cells is transported with each unit mass of
manure. To calculate the mass of manure eroded, empirical
constants from the work of Khaleel et al. (1979) were used.
The predicted range of faecal coliform concentrations was in
the range of approximately 1000–2500 CFU 100 ml)1.
Unfortunately, no comparison was made with observed data.
Other recent attempts at predicting faecal coliform
numbers transported in overland flow have focused on their
transport through catchments. For example, Tian et al.
(2002) describe the transport of E. coli as a function of
surface runoff volume and an empirical delivery ratio based
upon landscape factors; whereas Fraser et al. (1998) use a
largely conceptual model to calculate a loading rate of faecal
coliforms to streams. The model of Tian et al. (2002) was
tested against data from the Mangatoama study site, a
1Æ45 km2 predominately grazed catchment at the Whatawhata Research Centre, Hamilton, New Zealand. They found
that predicted and measured E. coli counts were typically
between 200 and 1300 CFU 100 ml)1, however, on one
occasion the sampled data were three times that of the model
output. Fraser et al. (1998) found that their model was
useful in being able to rank the relative risk of faecal
contamination from livestock in 12 watersheds in New York
State, ranging in size from 1Æ5 to 50 km2. However
correlation of predicted and observed faecal coliform
concentrations in river water (mean measured values in
the range 142 to 1657 CFU 100 ml)1) proved non-significant.
Such methods allow us to make predictions of pathogen
numbers transported to watercourses in overland flow, but
do not relate to the processes acting on pathogens at the soil
surface or after their entrainment in overland flow. In fact,
there is only a limited experimental basis for describing
these processes, but soil erosion science does at least offer a
framework for investigating them further.
4.2 Pathogen transport processes
4.2.1 Initial and boundary conditions. Before the detachment and transport of microorganisms can be discussed,
the initial and boundary conditions of the slurry-amended
soil needs to be described. Previous workers (Reddy et al.
1981; Yeghiazarian and Montemagno 2000) have attempted
to describe how the relationship between waste-derived
microorganisms and soil and waste particles. Figure 1
Microorganisms
attached to waste
Microorganisms
attached to soil particles
Free microorganisms
Fig. 1 Three likely states in which microorganisms are likely to exist
in a soil–slurry mixture
illustrates three possible states in which microorganisms are
likely to exist in a soil–slurry mixture, i.e.:
• attached to soil particles;
• attached to waste or slurry particles; and
• as unattached cells or clumps.
A description of the factors controlling the partitioning of
microorganisms between these different states does not
presently exist. It is also recognized that there may be
significant differences in partitioning associated with different microbial groups, e.g. bacteria and protozoa.
4.2.2 Initiation of overland flow. Overland flow occurs
either when the rainfall intensity exceeds the soil’s infiltration rate (infiltration excess overland flow); or when the soil
become saturated with water so that no further rainfall can
enter the soil (known as saturated overland flow). Once
overland flow has been generated, by whichever mechanism,
there is the potential for the rapid transport of microorganisms to surface waters.
4.2.3 Entrainment of microorganisms in overland
flow. Soil erosion scientists classically divide soil erosion
processes into three phases: detachment, transport and
deposition (Meyer and Wischmeier 1969). These phases can
occur as a result of the action of raindrops or the action of
flowing water or a combination of both. We can assume that
microorganisms positioned on the soil surface have the same
processes acting upon them as a soil particle.
The detachment of microorganisms by raindrops or
overland flow appears to have received very little attention.
However, we suggest that microbial detachment will depend
upon the properties of the microbial population and the
properties of the detaching agent. We would suggest that the
factors likely to affect the rate at which microorganisms are
ª 2003 The Society for Applied Microbiology, Journal of Applied Microbiology Symposium Supplement, 94, 87S–93S
PATHOGEN TRANSPORT IN OVERLAND FLOW
detached may include the number of microorganisms on the
soil surface; whether or not they are protected by soil or
biological material; how strongly they are adhered to particle
surfaces and to each other; the kinetic energy of the rainfall;
and the overland flow velocity and depth.
By combining Meyer and Wischmeier’s (1969) model
with the initial conditions as set out in Fig. 1 we can propose
three potential pathogen transport scenarios. Figure 2a
shows microorganisms as free cells within soil pore water or
water films on the soil surface. They are incorporated into
the flow as it passes over them. Those microorganisms
which are attached to soil or waste particles are entrained
when the force applied by the flow on the soil surface
exceeds the soil and waste particles resistance, or when they
are hit by rain drops which may propel them into the flow
(Fig. 2b). We expect that waste particles will have less
resistance to these entrainment processes as they would
typically be of lower density and only weakly consolidated.
For phosphorus, Quinton et al. (2001) demonstrated that
erosion processes were selective with proportionally more
fine, phosphorus-containing material being moved in small
runoff events. We can hypothesize that selective detachment
and transport of waste particles and associated microorganisms is also likely to occur because of their low density when
compared with soil mineral particles of the same size. The
third scenario is where cells are detached from soil or waste
particle surfaces by either raindrop impact or the flow itself
Flow
di
rect
ion
Soil
surfa
ce
Wate
r sur
fac e
i
i
(a)
ii
Soil
surfa
ce
Wate
ii
r sur
face
i
(b)
Wate
Soil
sur
face
ii
r sur
face
(c)
Fig. 2 Proposed pathogen transport scenarios: (a) shows the incorporation of free microorganisms in soil pores (i) and water films (ii) into
overland flow; (b) shows the entrainment of waste or soil particles into
overland flow as a result of raindrop (i) or flow (ii) detachment; (c)
shows the detachment of microorganisms from soil surfaces as a result
of raindrop (i) or flow (ii) detachment
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and transported as free cells (Fig. 2c). Given these processes,
the overland flow will contain a mix of microorganisms in
the three states identified in Fig. 2 and, as with microorganisms in the soil (Fig. 1), we know virtually nothing about
how microorganisms may be partitioned between these
states whilst in transport.
4.2.4 Transport and deposition. It is well established the
density and size of particles influences their settling velocity.
Small, low-density particles settle more slowly than those of
large, high density. For example, the low density of
microorganisms, approximately 1Æ1 g cm)3 (Paul and Clark
1996) and their small size (typically 1–2 lm), suggests that
once entrained they will remain in suspension. Similarly, it
would be expected that a bacterial cell that is strongly
adhered to a soil particle will not travel as far as one that is
floating freely in suspension. Therefore, to model the
deposition of microorganisms, it will be necessary to decide
on the proportion of microorganisms moving freely and
attached to particles, and how environmental factors, such as
flow conditions and soil conditions will influence these
proportions.
There is little evidence in the literature to support or
refute these simple hypotheses. Most studies have been
carried out in the field and have focused on the effectiveness
of particular control measures. Those measures designed to
trap microorganisms once entrained, such as vegetative filter
strips (VFS), have been shown to be highly variable in their
effectiveness. Coyne et al. (1998) show that between 55 and
95% of faecal coliforms and between 42 and 93% of faecal
streptococci are trapped by the VFS. These figures compare
with a much narrower range for sediment (95–99%). These
figures are of the same order as those reported by Hayes
et al. (1984) for sediment and Young et al. (1980) for faecal
coliforms. The lower bacterial trapping efficiencies of the
VFS support the argument that because of their lower
density, deposition is less likely for free-floating microorganisms once entrained than it would be for a soil particle of
similar size. If we assume that bacterial cells transported
freely move with the water and are not deposited, unless all
the water infiltrates, then we can also postulate that the
observed reduction in microorganism numbers is due to the
deposition of microorganisms associated with soil material.
If this is the case, then the variability in trapping efficiencies
reported by Coyne et al. (1998) may suggest variation in the
partitioning of microorganisms between water and suspended sediment particles.
5. CONCLUSIONS
There is evidence to suggest that faecal pollution of
watercourses from diffuse catchment sources occurs following storm events. This association with storm events
ª 2003 The Society for Applied Microbiology, Journal of Applied Microbiology Symposium Supplement, 94, 87S–93S
92S S . F . T Y R R E L A N D J . N . Q U I N T O N
suggests that rapidly responding hydrological pathways such
as overland flow are likely to be important. Empirically
based soil erosion models have been developed to predict
pathogen loads associated with overland flow transport.
These models are not intended to inform our understanding
of the transport processes themselves. Pathogen transport is
likely to be influenced by the initial conditions in slurryamended soil, i.e. the relationship between faecal microorganisms and soil and waste particles. A simple conceptual
description of these initial conditions is suggested in this
paper, but the fact remains that little has been published to
date on this subject. Using well-established soil erosion
process understanding we have attempted to describe the
mechanisms which would facilitate pathogen transport in
overland flow. Once again, there are only a relatively small
number of studies with which to test our hypotheses.
Further research is needed to properly test these hypotheses.
A better understanding the dynamics of microbial transport
will enable the development of better diffuse pollution
management approaches.
6. ACKNOWLEDGEMENTS
Financial support for our work on pathogen transport has
been provided by the Biotechnology and Biological Sciences
Research Council (BBSRC); grant number 63/MAF12260.
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PATHOGEN TRANSPORT IN OVERLAND FLOW
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